Stiffness-controlled three-dimensional extracellular matrices for high-resolution imaging of cell behavior

Nature Protocols

Volumn 7, Issue 11, 2012, Pages 2056-2066

  Fischer, Robert S ^a   Myers, Kenneth A ^b   Gardel, Margaret L ^c,d,e   Waterman, Clare M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b UNIVERSITY OF THE SCIENCES   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYACRYLAMIDE;

ARTICLE; CELL FUNCTION; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; EXTRACELLULAR MATRIX; INVESTIGATIVE PROCEDURES; METHODOLOGY; PRIORITY JOURNAL; RIGIDITY; THREE DIMENSIONAL EXTRACELLULAR MATRIX; TIME LAPSE IMAGING;

ACRYLIC RESINS; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELLULAR MICROENVIRONMENT; EXTRACELLULAR MATRIX; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MICROSCOPY, PHASE-CONTRAST;

EID: 84868089352     PISSN: 17542189     EISSN: 17502799     Source Type: Journal    
DOI: 10.1038/nprot.2012.127     Document Type: Article

References (76)

1. Ghosh, K., Thodeti, C.K., Dudley, A.C., Mammoto, A. & Klagsbrun, M. et al. Tumor-derived Ed.thelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. Proc. Natl. Acad. Sci. USA 105, 11305-11310 (2008
2. Ingber, D.E. Mechanical signaling and the cellular response to extracellular matrix in angiogenesis and cardiovascular physiology. Circ. Res. 91, 877-887 (2002 (Pubitemid 35373587)
3. Mammoto, A., Connor, K.M., Mammoto, T., Yung, C.W. & Huh, D. et al. A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457, 1103-1108 (2009
4. Discher, D.E., Janmey, P. & Wang, Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139 (2005
5. Pelham, R.J. Jr. & Wang, Y.L. Cell locomotion and focal adhesions are regulated by the mechanical properties of the substrate. Biol. Bull. 194, 348-349 (1998
6. Saez, A., Ghibaudo, M., Buguin, A., Silberzan, P. & Ladoux, B. Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc. Natl. Acad. Sci. USA 104, 8281-8286 (2007 (Pubitemid 47175479)
7. Beningo, K.A., Dembo, M. & Wang, Y.L. Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors. Proc. Natl. Acad. Sci. USA 101, 18024-18029 (2004 (Pubitemid 40054068)
8. Even-Ram, S., Doyle, A.D., Conti, M.A., Matsumoto, K. & Adelstein, R.S. et al. Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat. Cell Biol. 9, 299-399 (2007
9. Engler, A.J., Sen, S., Sweeney, H.L. & Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006 (Pubitemid 44233625)
10. Tilghman, R.W., Cowan, C.R., Mih, J.D., Koryakina, Y. & Gioeli, D. et al. Matrix rigidity regulates cancer cell growth and cellular phenotype. PLoS One 5, e12905 (2010
11. Wang, N., Naruse, K., Stamenovic, D., Fredberg, J.J. & Mijailovich, S.M. et al. Mechanical behavior in living cells consistent with the tensegrity model. Proc. Natl. Acad. Sci. USA 98, 7765-7770 (2001 (Pubitemid 32642635)
12. Lo, C.M., Wang, H.B., Dembo, M. & Wang, Y.L. et al. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144-152 (2000 (Pubitemid 30436733)
13. Kong, H.J., Liu, J., Riddle, K., Matsumoto, T. & Leach, K. et al. Non-viral genEd.livery regulated by stiffness of cell adhesion substrates. Nat. Mater. 4, 460-464 (2005 (Pubitemid 40774051)
14. Mammoto, A., Mammoto, T. & Ingber, D.E. Mechanosensitive mechanisms in transcriptional regulation. J. Cell Sci. 125, 3061-3073 (2012
15. lEd.c, Q., Shi, Q., Blonk, I., Sonnenberg, A. & Wang, N. et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-depEd.nt manner. J. Cell Biol. 189, 1107-1115 (2010
16. Baker, E.L., Lu, J., Yu, D., Bonnecaze, R.T. & Zaman, M.H. et al. Cancer cell stiffness: Integrated roles of threEd.mensional matrix stiffness and transforming potential. Biophys. J. 99, 2048-2057 (2010
17. Baker, R., Rogers, K.D., Sheph Ed. N. & Stone, N. New relationships between breast microcalcifications and cancer. Br. J. Cancer 103, 1034-1039 (2010
18. Egeblad, M., Rasch, M.G. & Weaver, V.M. Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22, 697-706 (2010
19. Wang, Y.L. & Pelham, R.J. Jr. Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol. 298, 489-496 (1998 (Pubitemid 28450775)
20. Frey, M.T., Engler, A., Discher, D.E., Lee, J. & Wang, Y.L. Microscopic methods for measuring the elasticity of gel substrates for cell culture: Microspheres, microindenters, and atomic force microscopy. Methods Cell Biol. 83, 47-65 (2007
21. Weigelt, B., Lo, A.T., Park, C.C., Gray, J.W. & Bissell, M.J. HER2 signaling pathway activation and response of breast cancer cells to HER2-targeting agents is depEd.nt strongly on the 3D microenvironment. Breast Cancer Res. Treat. 122, 35-43 (2009
22. Dunn, J.C., Tompkins, R.G. & Yarmush, M.L. Hepatocytes in collagen sandwich: Evidence for transcriptional and translational regulation. J. Cell Biol. 116, 1043-1053 (1992
23. Dunn, J.C., Yarmush, M.L., Koebe, H.G. & Tompkins, R.G. Hepatocyte function and extracellular matrix geometry: Long-term culture in a sandwich configuration. FASEB J. 3, 174-177 (1989
24. Erler, J.T. & Weaver, V.M. ThreEd.mensional context regulation of metastasis. Clin. Exp. Metastasis 26, 35-49 (2009
25. Pankov, R., Ed., Y., Even-Ram, S., Araki, M. & Clark, K. et al. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170, 793-802 (2005
26. Petrie, R.J., Doyle, A.D. & Yamada, K.M. Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10, 538-549 (2009
27. Beningo, K.A. & Wang, Y.L. Double-hydrogel substrate as a model system for threEd.mensional cell culture. Methods Mol. Biol. 370, 203-212 (2007
28. RehfEd., F., Brown, A.E., Raab, M., Cai, S. & Zajac, A.L. et al. Hyaluronic acid matrices show matrix stiffness in 2D and 3D dictates cytoskeletal order and myosin-II phosphorylation within stem cells. Integr. Biol. (Camb.) 4, 422-430 (2012
29. Ezzell, R.M., Toner, M., HEd.icks, K., Dunn, J.C. & Tompkins, R.G. et al. Effect of collagen gel configuration on the cytoskeleton in cultured rat hepatocytes. Exp. Cell Res. 208, 442-452 (1993 (Pubitemid 23299128)
30. Myers, K.A., Applegate, K.T., Danuser, G., Fischer, R.S. & Waterman, C.M. et al. Distinct ECM mechanosensing pathways regulate microtubulEd.namics to control Ed.thelial cell branching morphogenesis. J. Cell Biol. 192, 321-334 (2011
31. Harunaga, J.S. & Yamada, K.M. Cell-matrix adhesions in 3D. Matrix Biol. 30, 363-369 (2011
32. Shakesheff, K.M. & Rose, F.R. Tissue engineering in thEd.velopment of replacement technologies. Adv. Exp. Med. Biol. 745, 47 (2012
33. Huh, D., Hamilton, G.A. & Ingber, D.E. From 3D cell culture to organs-on-chips. TrEd. Cell Biol. 21, 745-754 (2011
34. Hutmacher, D.W., Horch, R.E., Loessner, D., Rizzi, S. & Sieh, S. et al. Translating tissue engineering technology platforms into cancer research. J. Cell Mol. Med. 13, 1417-1427 (2009
35. Maltman, D.J. & Przyborski, S.A. Developments in threEd.mensional cell culture technology aimed at improving the accuracy of in vitro analyses. Biochem. Soc. Trans. 38, 1072-1075 (2010
36. Pathak, A. & Kumar, S. IndepEd.nt regulation of tumor cell migration by matrix stiffness and confinement. Proc. Natl. Acad. Sci. USA 109, 10334-10339 (2012
37. Huh, D., Matthews, B.D., Mammoto, A., Montoya-Zavala, M. & Hsin, H.Y. et al. Reconstituting organ-level lung functions on a chip. Science 328, 1662-1668 (2011
38. Raeber, G.P., Lutolf, M.P. & Hubbell, J.A. Molecularly engineered PEG hydrogels: A novel model system for proteolytically mediated cell migration. Biophys. J. 89, 1374-1388 (2005 (Pubitemid 41099019)
39. Mikos, A.G., Bao, Y., Cima, L.G., Ingber, D.E. & Vacanti, J.P. et al. Preparation of poly(glycolic acid) bonded fiber structures for cell attachment and transplantation. J. Biomed. Mater. Res. 27, 183-189 (1993 (Pubitemid 23027517)
40. Mikos, A.G., Sarakinos, G., Lyman, M.D., Ingber, D.E. & Vacanti, J.P. et al. Prevascularization of porous biodegradable polymers. Biotechnol. Bioeng. 42, 716-723 (1993 (Pubitemid 23257725)
41. Miller, J.S., Stevens, K.R., Yang, M.T., Baker, B.M. & Nguyen, D.H. et al. Rapid casting of patterned vascular networks for perfusable engineered threEd.mensional tissues. Nat. Mater. 9, 768-774 (2012
42. Cukierman, E. & Bassi, D.E. Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin. Cancer Biol. 20, 139-145 (2010
43. Grinnell, F. & Petroll, W.M. Cell motility and mechanics in threEd.mensional collagen matrices. Annu. Rev. Cell Dev. Biol. 26, 335-361 (2009
44. Hakkinen, K.M., Harunaga, J.S., Doyle, A.D. & Yamada, K.M. Direct comparisons of the morphology, migration, cell adhesions, and actin cytoskeleton of fibroblasts in four different threEd.mensional extracellular matrices. Tissue Eng. Part A 17, 713-724 (2010
45. Miron-MEd.za, M., Seemann, J. & Grinnell, F. ThEd.fferential regulation of cell motile activity through matrix stiffness and porosity in threEd.mensional collagen matrices. Biomaterials 31, 6425-6435 (2010
46. Levental, K.R., Yu, H., Kass, L., Lakins, J.N. & Egeblad, M. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009
47. Fischer, R.S., Gardel, M., Ma, X., Adelstein, R.S. & Waterman, C.M. Local cortical tension by myosin II guides 3D Ed.thelial cell branching. Curr. Biol. 19, 260-265 (2009
48. Carmeliet, P., De Smet, F., Loges, S. & Mazzone, M. Branching morphogenesis and antiangiogenesis candidates: Tip cells lEd.the way. Nat. Rev. Clin. Oncol. 6, 315-326 (2009
49. Mammoto, A., Mammoto, T. & Ingber, D.E. Rho signaling and mechanical control of vascular development. Curr. Opin. Hematol. 15, 228-234 (2008 (Pubitemid 351507576)
50. Buxboim, A. & Discher, D.E. Stem cells feel thEd.fference. Nat. Methods 7, 695-697 (2010
51. Trappmann, B., Gautrot, J.E., Connelly, J.T., Strange, D.G. & Li, Y. et al. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11, 642-649 (2012
52. Myers, J.P. & Gomez, T.M. Focal adhesion kinase promotes integrin adhesion dynamics necessary for chemotropic turning of nerve growth cones. J. Neurosci. 31, 13585-13595 (2011
53. Myers, J.P., Santiago-Medina, M. & Gomez, T.M. Regulation of axonal outgrowth and pathfinding by integrin-ECM interactions. Dev. Neurobiol. 71, 901-923 (2011
54. Renaudin, A., Lehmann, M., Girault, J. & McKerracher, L. Organization of point contacts in neuronal growth cones. J. Neurosci. Res. 55, 458-471 (1999 (Pubitemid 29110553)
55. Robles, E. & Gomez, T.M. Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat. Neurosci. 9, 1274-1283 (2006 (Pubitemid 44454269)
56. Santiago-Medina, M., Myers, J.P. & Gomez, T.M. Imaging adhesion and signaling dynamics in Xenopus laevis growth cones. Dev. Neurobiol. 72, 585-599 (2012
57. Jiang, F.X., Yurke, B., Schloss, R.S., Firestein, B.L. & Langrana, N.A. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng. Part A 16, 1873-1889 (2010
58. Leach, J.B., Brown, X.Q., Jacot, J.G., Dimilla, P.A. & Wong, J.Y. Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity. 4, 26-34 (2007
59. Kubow, K.E. & Horwitz, A.R. Reducing background fluorescence reveals adhesions in 3D matrices. Nat. Cell Biol. 13, 3-5 (2011
60. Geiger, B., Spatz, J.P. & Bershadsky, A.D. Environmental sensing through focal adhesions. Nat. Rev. Mol. Cell Biol. 10, 21-33 (2009
61. Doyle, A.D., Wang, F.W., Matsumoto, K. & Yamada, K.M. OnEd.mensional topography underlies threEd.mensional fibrillar cell migration. 184, 481-490 (2009
62. Fraley, S.I., Feng, Y., Krishnamurthy, R., Kim, D.H. & Celedon, A. et al. A distinctive role for focal adhesion proteins in threEd.mensional cell motility. Nat. Cell Biol. 12, 598-604 (2010
63. Hakkinen, K.M., Harunaga, J.S., Doyle, A.D. & Yamada, K.M. Direct comparisons of the morphology, migration, cell adhesions, and actin cytoskeleton of fibroblasts in four different threEd.mensional extracellular matrices. Tissue Eng. Part A 17, 713-724 (2011
64. Wang, N., Tytell, J.D. & Ingber, D.E. Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82 (2009
65. Wadsworth, P. Using cultured mammalian cells to study mitosis. Cold Spring Harb. Protoc. 2012, 205-212 (2012
66. Yeung, T. et al. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34 (2005 (Pubitemid 40066224)
67. Buxboim, A., Rajagopal, K., Brown, A.E. & Discher, D.E. How deeply cells feel: Methods for thin gels. J. Phys. Condens. Matter 22, 194116 (2010
68. Guo, W.H. & Wang, Y.L. in Live Cell Imaging: A Laboratory Manual (eds. Goldman, R.D., Swedlow, J.R., Spector, D.L.) 43 (Cold Spring Harbor, 2010
69. Rieder, C.L. & Hard, R. Newt lung epithelial cells: Cultivation, use, and advantages for biomedical research. Int. Rev. Cytol. 122, 153-220 (1990 (Pubitemid 20374371)
70. Lutz, D.A., Hamaguchi, Y. & Inoue, S. Micromanipulation studies of the asymmetric positioning of the maturation spindle in Chaetopterus sp. oocytes: I. Anchorage of the spindle to the cortex and migration of a displaced spindle. Cell Motil. Cytoskeleton 11, 83-96 (1988
71. Phillips, J.B., Bunting, S.C., Hall, S.M. & Brown, R.A. Neural tissue engineering: A self-organizing collagen guidance conduit. Tissue Eng. 11, 1611-1617 (2005 (Pubitemid 41636445)
72. Olsen, B.R. Life without perlecan has its problems. J. Cell Biol. 147, 909-912 (1999
73. Avery, N.C., Sims, T.J. & Bailey, A.J. QuantitativEd.termination of collagen cross-links. Methods Mol. Biol. 522, 103-121 (2009
74. Slatter, D.A., Avery, N.C. & Bailey, A.J. Collagen in its fibrillar state is protected from glycation. Int. J. Biochem. Cell Biol. 40, 2253-2263 (2008
75. Waterman-Storer, C.M. Microtubule/organelle motility assays. Curr. Protoc. Cell Biol. 13, 13.1.1-13.1.21 (2001
76. Omidian, H., Rocca, J.G. & Park, K. Advances in superporous hydrogels. J. Control Release 102, 3-12 (2005) (Pubitemid 40093771)